SUMMARY

Using a newly developed data logger to measure acceleration, we demonstrate
that free-ranging king and Adélie penguins only beat their flippers
substantially during the first part of descent or when they were presumed to
be chasing prey at the bottom of dives. Flipper beating stopped during the
latter part of ascent: at 29±9 % (mean ± S.D.) of dive depth
(mean dive depth=136.8±145.1 m, N=425 dives) in king penguins,
and at 52±20 % of dive depth (mean dive depth=72.9±70.5 m,
N=664 dives) in Adélie penguins. Propulsive swim speeds of
both species were approximately 2 m s-1 during dives; however, a
marked increase in speed, up to approximately 2.9 m s-1, sometimes
occurred in king penguins during the passive ascending periods. During the
prolonged ascending, oblique ascent angle and slowdown near the surface may
represent one way to avoid the potential risk of decompression sickness.
Biomechanical calculations for data from free-ranging king and Adélie
penguins indicate that the air volume of the birds (respiratory system and
plumage) can provide enough buoyancy for the passive ascent. When comparing
the passive ascents for shallow and deep dives, there is a positive
correlation between air volume and the depth of the dive. This suggests that
penguins regulate their air volume to optimize the costs and benefits of
buoyancy.

Introduction

Penguins are outstanding breath-hold divers. Despite their small body mass,
Adélie penguins Pygoscelis adeliae (4-5 kg) dive up to 180 m
depth and may remain submerged for 4 min
(Naito et al., 1990;
Watanuki et al., 1997) and
king penguins Aptenodytes patagonicus (10-12 kg) dive to over 300 m
and for up to 7 min (Kooyman et al.,
1992). Particularly intriguing is the observation that penguins
seem to dive on inspiration (Kooyman et
al., 1971), which no doubt contributes to increasing oxygen stores
but obviously increases buoyant resistance at shallow depths and risk of
decompression sickness. Air in the body makes divers buoyant. Several studies
have concluded that buoyant force is a major load for shallow diving birds
(Dehner, 1946;
Stephenson et al., 1989;
Lovvorn et al., 1991; Lovvorn
and Jones,
1991a,b;
Wilson et al., 1992;
Stephenson, 1994). Air volume
in the body is difficult to measure in free diving animals. Stephenson
(1994) measured buoyancy in
unrestrained shallow diving birds in a tank. However, this method is
impossible to use for deep-diving birds such as penguins. Furthermore,
buoyancy should change with ambient pressure at each depth, and work against
buoyancy is expected to vary throughout diving. Metabolic rate in the
locomotory muscles, which affects oxygen store depletion, is indirectly
dependent on swim speed and directly dependent on flipper stroke effort
(Kooyman and Ponganis, 1998),
but no method has been devised for measuring their flipper movements under
natural conditions. Detailed studies on underwater movement of penguins have
remained limited to observations of birds close to the sea surface
(Kooyman et al., 1971) or in
aquaria (Clark and Bemis,
1979).

For swimming penguins, the periodic alternation of up- and down-strokes of
the flippers induce oscillations of the body. This involves acceleration and
deceleration with each propulsive stroke
(Clark and Bemis, 1979;
Bannasch, 1995). To investigate
the fine-scale movements of penguins in unrestrained dives under natural
conditions, we developed an acceleration data logger
(Yoda et al., 1999).
Propulsive beating of the flippers, depth and swim speed were recorded every
second from Adélie and king penguins diving at sea. Using these data,
we first determined some diving characteristics of penguins, especially of
their flipper movements. Secondly, air volume in the body was estimated for
each dive of Adélie and king penguins using a biomechanical model.
Finally, the results are discussed in terms of biomechanical and physiological
constraints on optimal diving strategies.

Materials and methods

Data loggers

The detailed behaviors of penguins were monitored using a data logger with
8-bit resolution that recorded depth and acceleration once every second
(NIPR-400D2G: 42.7 g, 19 mm diameter, 90 mm length; Little Leonardo, Tokyo,
Japan). Depth resolution was 1.56 m. The logger has a piezo-resistive
accelerometer (Model 3031, IC Sensors) with filtering of the analog sensor
signal by a band-pass filter of 0.53-64 Hz. The amplitude of accelerations was
stored as an integrated value during the sampling interval of 1 s. The
measuring range of the device was 0-11.8 m s-2. The logger was
attached to the back of a penguin to record the deceleration component of
movements together with the long axis of the body. According to our
investigations in aquaria using the acceleration data logger attached to
captive penguins, the measured deceleration of gliding birds is lower than
0.098 m s-2; we used this value to define the threshold for
cessation of flipper beating.

Swim speed and depth were measured using a 12-bit resolution
speed/depth/temperature (PDT) data logger (UWE-200PDT for Adélie: 59.2
g, 20 or 23 mm diameter at the thickest part, 120 mm length; KS-400PDT for
king: 81.5 g, 25 or 32 mm diameter at the thickest part, 110 mm length;
sampling interval 1 s; Little Leonardo, Tokyo, Japan). The depth ranges were
0-200 m (resolution 0.05 m, for UWE-200PDT) or 0-400 m (resolution 0.1 m, for
KS-400PDT). Any recorded pressure values exceeding 2 m in depth were
considered to constitute a dive. Maximum depth during a dive was represented
as a dive depth. Swim speed was measured by counting the revolutions of a
propeller (RPS; revs s-1) and converting to speed using depth
versus RPS calibration data collected from the same animals (see
Blackwell et al., 1999;
Yoda et al., 1999). The
calibration lines were obtained from each logger with coefficients of
determination higher than 0.97 within a speed range of 1.2-2.8 m
s-1 for two king penguins and 0.6-2.2 m s-1 for two
Adélie penguins. RPS values were not converted to speed when they were
lower than the stall RPS (0.3 m s-1) of the instrument, as
determined experimentally.

Field experiments

The studies were carried out on Possession Island (46.4 °S, 51.8°
E, Crozet Archipelago) during part of the breeding season of king penguin
Aptenodytes patagonicu (Miller) (February—March, 1996) and on
Ile des Pétrels, Dumont d'Urville station, Adélie Land (66.7°
S, 140.0 °E) during the Adélie penguin Pygoscelis
adeliae (Hombron and Jacquinot) breeding season (December,
1996—February, 1997).

The loggers were attached caudally to the back to minimize drag
(Bannasch et al., 1994;
Culik et al., 1994a), using
plastic cable ties and adhesive at Dumont d'Urville and Tesa tape at Crozet.
On removal of the loggers, the cable ties and tape were also removed from the
birds. The remaining adhesive would fall off with the feathers at molt. Five
king penguins were equipped with both PDT and D2G loggers, of which two sets
were recovered with reliable data (see
Ropert-Coudert et al., 2000
for detailed information). Seven Adélie penguins were equipped with D2G
loggers, and other three birds were equipped with both PDT and D2G loggers.
Adélie penguins were caught following their return from foraging trips,
and the loggers were retrieved (see Yoda
et al., 1999, for detailed information).

Biomechanical model

The data obtained from free-ranging penguins were analyzed using a
biomechanical model, which was modified from a model used for flying birds
(Azuma, 1997). Three forces act
on an ascending, gliding penguin when flipper beating has ceased
(Fig. 1). At ascent angleθ
, changes in speed U along the swimming path are determined by
the difference between the drag FD and the component of
the buoyancy FB parallel to the path of swimming
(FBsinθ) (Fig.
1). Changes in ascent angle θ are determined by the
difference between the downward lift FL and the component
of the buoyancy FB perpendicular to the path of swimming
(FBcosθ) (Fig.
1). These relationships are described by the following equations.
1
and
2
where m is the measured body mass (kg) of the birds and t is
the time (s). The added mass (Daniel,
1984; Vogel, 1994)
was not included with the body mass, assuming a quasi-steady flow around the
gliding penguin, in which swimming motions are absent and changes in speed are
not abrupt. The ascent angle θ was calculated from measured swim speed
and vertical speed, the latter variable being calculated from the rate of
change of depth. In model calculations, buoyancy FB was
adjusted for the compression of air spaces with depth using the following
equation, which is modified from Wilson et al.
(1992):
3
where g is the gravitational constant (9.807 m s-2),ρ
w is the density of the sea water (1.027×103 kg
m-3 at 10 °C; Kooyman,
1989), ρt is the density of penguin body tissue
(1.02×103 kg m-3;
Wilson et al., 1992),
Va0 is the initial air volume (m3) kept in the
respiratory system and trapped in feathers at depth D0,
the point at which the penguins cease flipper beating, Ps
is atmospheric pressure at the surface (1.013×105 Pa; 1 atm)
and D is depth. The total drag FD increases with
speed and was calculated using following equation:
4
where S is a reference area and CD is the drag
coefficient. In the model calculation, the estimated wetted surface area
(0.3269m2) and CD (0.003;
Clark and Bemis, 1979) are used
for king penguins. For Adélie penguins, we used
CD=0.0368 (Culik et
al., 1994b) and the cross-sectional area of the body at its widest
point, which was calculated from the measured girth of each bird. The first
term on the right in equation 4 is the drag, including the parasite drag of
the body and the profile drag of the wings. The drag coefficients
CD of both species were derived from decelerative gliding
or swim canal measurements using living penguins
(Clark and Bemis, 1979;
Culik et al., 1994b). In the
model calculation, CD was assumed to be constant
(discussed below). The second term on the right is the induced drag, which
arises when the wings produce lift. Downward lift FL was
assumed to be generated by the outstretched flippers at negative angle of
attack. Lift on the body itself was not considered. When
SW is taken to be the wing area
(8.71×10-3 m2 for Adélie,
20.28×10-3 m2 for king;
Osa, 1994),
CL the lift coefficient, which varies with angle of attack
of the flipper, and AR the effective aspect ratio (7.28 for
Adélie, 9.66 for king; Osa,
1994), the downward lift FL was calculated
using the equation:
5
Substituting each force (FB, FD,
FL) in equations 1 and 2 by equations 3-5, respectively,
gives two equations with two unknown variables, U and
CL. The model simulation was conducted for each dive under
several values of initial air volume Va0. The simulated
speeds were then compared with measured speed to select an appropriate value
of the initial air volume for each dive.

Schematic diagram showing ascending angle (θ), buoyancy
(FB), drag (FD) and downward lift
(FL) acting on an ascending, gliding king penguin with a
data logger attached. This photograph was taken at an aquarium.

Results are presented as means ± S.D. Correlations between variables
were tested using the Spearman rank correlation coefficient. Results were
considered significant at P<0.05.

Results

The equipped king penguins conducted multiple deep dives with mean dive
depth being 50.3±76.4 m (N=1428 dives, 2 birds) and maximum
dive depths being 283.8 m for the 9.7 kg bird and 318.4 m for the 11.5 kg
bird. Mean dive duration was 144.0±126.2 s (N=1428 dives, 2
birds) and maximum dive durations were 449 s for the 9.7 kg bird and 453 s for
the 11.5 kg bird. Adélie penguins had a mean mass of 4.6 kg (10 birds;
range 4.0-5.1 kg). The total number of dives recorded was 4067. Mean dive
depth was 37.3±32.0 m and maximum dive depth for each bird varied from
65.6 m for a 4.0 kg bird to 145.9 m for a 4.8 kg bird. Mean dive duration was
80.7±46.6 s and maximum dive duration varied from 121 s for a 4.2 kg
bird to 206 s for a 4.5 kg bird.

According to the acceleration data, flipper movements were substantial
during the early descent in every dive made by the penguins
(Fig. 2). However, birds
stopped beating their flippers during the final stages of the ascent
(Fig. 2). Although there was
apparently some active propulsion in the late ascent of some dives, which
could be attributed to pursuit of prey, all penguins exhibited cessation of
flipper beating during the ascent (N=664 dives, 10 Adélies;
N=425 dives, 2 kings). The depth at which this occurred differed
between dives and individuals. Fig.
2A illustrates the V-shaped dives of an Adélie penguin,
which stopped beating its flippers at a depth of 50 m after having descended
to approximately 120m. Fig. 2B
shows a second Adélie penguin that stopped beating its flippers at
around 30 m depth, i.e. close to the bottom of its trapezoid-shaped dives. The
mean depth at which Adélie penguins stopped beating their flippers
corresponded to an average of 52±20 % of the dive depth (10 birds, 664
dives, mean dive depth=72.9±70.5 m).
Fig. 2C shows dives of a king
penguin. King penguins stopped beating their flippers at an average of
29±9 % of dive depth (2 birds, 425 dives, mean dive
depth=136.8±145.1 m). Fig.
3 shows the relationships between dive depth and the depth of
flipper beat cessation. The ten Adélie penguins tended to cease their
flipper beating closer to the dive bottom than did the two king penguins
(Fig. 3A). The depths of
flipper beat cessation expressed as a percentage of dive depth were
significantly, but weakly, related to dive depth in both Adélie
(Spearman r=0.08, P<0.05) and king penguins (Spearman
r=-0.46, P<0.0001)
(Fig. 3B).

Relationships between dive depth and depth of flipper beat cessation in two
king penguins (filled circles) and ten Adélie penguins (open
triangles). Depths of flipper beat cessation are plotted as absolute depth (A)
and as a percentage of dive depth (B).

The propulsive swim speeds of king and Adélie penguins were about 2
m s-1 during dives. For all deep dives (i.e. over 50 m depth;
N=181 dives) of the king penguin, a marked increase in speed, up to
approx. 2.9 m s-1 in the most extreme case, occurred after flipper
beating stopped (Fig. 2C). This
increase in speed occurred for both king penguins (2 birds, 317 dives). In
case of another king penguin, where acceleration data were not obtained
because the memory of D2G logger was full, the depths at which the bird ceased
flipper beating were determined from the increase in swim speed. When
Adélie penguins stopped beating their flippers their speed also
sometimes increased (26 times in 1454 dives), but less markedly than for king
penguins. In the most extreme case, swim speed increased from 1.8 to 2.3 m
s-1.

The model simulation analysis was conducted for the passive ascent periods
of two king penguins and two Adélie penguins, from which a reliable
swim speed was recorded. An example of the simulation results for a king
penguin is shown in Fig. 4A.
The simulated speed under the condition of Va0=0.21
initial air volume at 52.9m depth (6.3 atm; 1
atm=1.013×105Pa), when the bird stopped flipper beating,
accords well with the measured speed (Fig.
4A). The initial air volume Va0 is the
equivalent of 1.21 at the surface (1 atm). It indicates that the king penguin
could ascend passively if 1.21 (1 atm) of air was retained in the body.
Indeed, the simulated speed fits well with the measured speed in every dive,
except for the final part of the ascent. Here, the simulated speed becomes
much higher than the measured speed. The measured decompression ratio
(Pt/Pt-1; the ambient pressure at time
t divided by the pressure 1 s before) never went lower than 0.8 in
any dive of either species. But simulated decompressions are rapid near the
surface because of the increase in simulated swim speed
(Fig. 4). Calculated lift
coefficients CL were nearly constant throughout the
passive ascent periods in both species, except for the final parts
(Fig. 4).
Fig. 4B is one example of the
model simulations for an Adélie penguin. An appropriate value of the
initial air volume is the equivalent of 0.91 at the sea surface (1 atm) for
the dive in question (Fig. 4B),
with the model simulation indicating that the bird could ascend passively if
0.91 (1 atm) of air was kept in the body.

Relationship between measured speed (thick black line) and simulated speed
(colored dots and lines) during the passive ascent periods of a king penguin
(A) and an Adélie penguin (B). Values beside the lines are air volume
(1) that might be kept by birds ascending passively (1 atm) used in the model
simulation. Measured decompression ratio and ascent angles are shown as thick
black lines. Simulated decompression ratios and lift coefficients are also
shown (colored dots and lines), assuming that each bird had 1.2 (A) or 0.9
litres (B) of air (1 atm). The depths at which the birds stopped flipper
beating are indicated.

The air volumes kept by penguins were estimated for each dive
(N=74 dives, 2 king penguins; N=40 dives, 2 Adélie
penguins). Their estimated air volumes range from 0.43 to 1.71 1 for king
penguins and from 0.38 to 0.911 for Adélie penguins, respectively.
There are significant positive relationships (P<0.05) between dive
depth and the estimated air volume for each bird
(Fig. 5,
Table 1).

Relationship between dive depth and estimated air volume of two king
penguins (A) and two Adélie penguins (B). Horizontal lines, calculated
from body mass using a equation in Lasiewski and Calder
(1971), indicate the expected
air volumes of the respiratory system for each penguin.

Discussion

Wing beat and passive ascending

The initial vigorous flipper beating of descending penguins demonstrates
hard work against positive buoyancy at shallow depths. Conversely, cessation
of flipper beating during the latter part of ascent indicates that penguins
then ascend passively. Thus, diving behavior is clearly affected by buoyancy.
Buoyancy can act as a resistance to downward movement but contributes to save
energy when ascending. Swimming penguins glide between strokes to reduce drag
costs (Clark and Bemis, 1979)
because drag associated with thrust motion is several times greater than would
be expected for the gliding phase
(Lighthill, 1971). A passive
ascent with prolonged gliding could be expected to reduce drag costs.

A passive ascent has been observed in shallow-diving birds such as the
great cormorant Phalacrocorax c. carbo, canvasback Aythya
valisineria, lesser scaup Aythya affinis and ruddy duck
Oxyura jamaicensis (Ross,
1976; Tome and Wrubleski,
1988; Stephenson et al.,
1989; Lovvorn,
1994). Lovvorn et al.
(1999) assumed in their model
that guillemots Uria lomvia would stop upward swimming to minimize
total cost. Wilson and Wilson
(1995) suspected that African
penguins Spheniscus demersus may partly surface passively because of
the increase in their measured swim speed. However, there has been no direct
measurement of flipper movement in deep-diving penguins under natural
conditions. The present study is a first report of extended periods of gliding
in ascending penguins.

Slowdown near the surface

The propulsive swim speed was approximately 2 m s-1 during
dives, independent of dive depth and species. This is consistent with the
speed of king penguins measured using another type of data logger
(Kooyman et al., 1992), and
accords well with the optimal speed for minimum cost of transport found in
each species (1.8-2.2 m s-1 for king,
Culik et al., 1996; 1.7-2.3 m
s-1 for Adélie, Culik and
Wilson, 1991). When ascending, both penguins stopped beating their
flippers and swim speed sometimes increased beyond the optimal speed.

Biomechanical calculations, together with data obtained from free-ranging
penguins, yield important insights into the movements of these birds during
the passive ascent periods. The model simulations indicate that the passive
ascent of penguins can be attributed to increased buoyancy from the expanding
air volume in the body. From Fig.
4A, the simulated speed matches the measured speed up to 27 s,
after which it becomes much higher than the measured speed. Similar results
were obtained from all other simulations in both species. The discrepancy
suggests that the penguins actually decelerated speed by some means, possibly
correlated to an increase in the profile drag of the flippers or parasite drag
of the body. Fig. 4 indicates
that the calculated lift coefficients suddenly increase during the final part
of ascent, suggesting that penguins might increase the attack angle of their
flippers, and thus increase the profile drag coefficient
(Vogel, 1994). Except for the
final part, lift coefficients were nearly constant throughout the ascent
(Fig. 4), supporting the
assumption that the drag coefficient (including profile drag) remains constant
during most of the passive ascent. Penguins could also increase the parasite
drag of the body. As has been observed for an emperor penguin Aptenodytes
forsteri coming to the surface, the feet can be turned down into the
normal standing posture to act as a brake
(Kooyman et al., 1971).
Penguins might also reduce speed by exhaling the air to decrease buoyancy, as
can be seen in a photograph of a surfacing Adélie penguin
(Kooyman, 1975).

Oblique ascent angle

Ascent angles were not vertical and became shallower the closer the bird
was to the surface (Fig. 4).
According to equation 2, ascent angle is affected by buoyancy and downward
lift. Penguins can control the ascent angle via the lift coefficient
mediated by the attack angle of their flippers. If penguins kept the ascent
angle steep and did not brake near the surface, then buoyancy would take them
rapidly to the surface without flipper stroke effort. For example, the king
penguin in Fig. 4A could reduce
the 38 s ascent duration by 13 s by ascending vertically. Therefore, the
oblique ascent angle and braking near the surface seem to be energetically
expensive and do not accord with optimal diving theory predicting that animals
maximize the proportion of time spent at the foraging depth
(Kramer, 1988;
Ydenberg and Clark, 1989). Why
then might the birds delay a prompt return to the surface?

Wilson et al. (1996)
hypothesized that an oblique ascent angle allows the birds to search both the
vertical and horizontal components of the water column. Results showing that
ascent angles during feeding dives were greater than during non-feeding dives
in Adélie penguins support the searching hypothesis
(Ropert-Coudert et al.,
2001b). However, the ascent angles became shallower nearer to the
surface (Ropert-Coudert et al.,
2001b), where the probability of prey acquisition should be low
because ingestion events (detected as abrupt decreases in oesophageal
temperature) were mostly observed at depths greater than than 40 m
(Ropert-Coudert et al.,
2001a). Hence, it seems unlikely that searching for prey can
explain the oblique ascent angle.

There may be physiological reasons why the penguins delay their ascent
time. Seals are known to exhale air before diving, and the free-swimming
Weddell seal Leptonychotes weddellii protects itself from nitrogen
narcosis and decompression sickness by limiting blood nitrogen uptake through
alveolar collapse (Falke et al.,
1985), but how deep-diving birds avoid the bends is not clear
(Kooyman and Ponganis, 1997).
The bird's lung may not collapse during a dive; blood nitrogen tensions in
Adélie penguins during simulated dives to 68m rose to levels that were
borderline for decompression sickness
(Kooyman et al., 1973),
leading the authors to suggest that shallow-diving penguins such as
Adélies and gentoos Pygoscelis papua avoid the risk of
elevated partial pressure of dissolved nitrogen by making short, shallow
dives. Ponganis et al. (1999)
suggested that king penguins have adapted to deep diving by reducing their
respiratory air volume compared to that in shallow-diving penguins. Indeed,
the measured air volume (69 ml kg-1;
Ponganis et al., 1999),
including respiratory and plumage air, of restrained king penguins during
simulated dives of up to 136m was much smaller than in shallow-diving
Adélie penguins of similar body size (165 ml kg-1;
Kooyman et al., 1973).
Similarly we found that the maximum mass-specific total air volume (125 ml
kg-1; calculated from Fig.
5A) of king penguins was smaller than that of Adélie
penguins (200 ml kg-1; calculated from
Fig. 5B). It is still unclear
how these birds avoid the risk of decompression sickness, because free-ranging
king penguins frequently repeat dives that are deeper and longer than the
simulated dives of 136m depth. As indicated by Kooyman et al.
(1973), use of short and
shallow dives only may not completely avoid the hazards of inert gas
absorption in Adélie penguins. It is known that symptoms characteristic
of decompression sickness can occur in man even after repetitive breath-hold
dives of short duration to shallow (15-20 m) depths
(Paulev, 1965).

Thus, there still seems to be a potential risk of decompression sickness in
free-ranging Adélie and king penguins.
Fig. 4 shows that measured
decompression was actually kept moderate because birds actively reduced their
rate of change of depth. Therefore, the oblique ascent angle and slowdown near
the surface could be one way to avoid potential decompression sickness; other
hypothetical mechanisms include a reduced cardiac output or a pressure-induced
restriction of pulmonary gas exchange
(Ponganis et al., 1999),
although there is no evidence to conclusively support any of these hypotheses
at present.

Air volume in the body

Whether animals dive on inspiration or expiration is important because
buoyant resistance is determined by the total air volume kept in the body.
However, air volume is difficult to measure in freely diving birds in the
laboratory (Stephenson, 1995),
and no methods have been devised for measuring them in the field
(Lovvorn et al., 1999).
Stephenson (1994) first
measured buoyancy in unrestrained shallow-diving lesser scaup Aythya
affinis, using a 1.52m deep tank. However, the same method is impossible
to use for deep-diving birds such as penguins. In the present study we
therefore estimated the total air volume (including respiratory system and
feathers) using data on depth, speed and acceleration, these being the first
data obtained from free-ranging penguins. The air volume of the respiratory
system was calculated to be 0.57 and 0.631 for 4.0 kg and 4.5 kg Adélie
penguins, respectively, and 1.27 and 1.481 for 9.7 kg and 11.5 kg king
penguins, respectively, using the analysis of Lasiewski and Calder
(1971). The estimated total
air volume for each species was similar to the expected respiratory volumes
for diving birds (Fig. 5),
which suggests that the biomechanical simulations yield good estimates of
respiratory air volume in the birds, although we did not have direct data of
the amount of air present in the feathers.

Ponganis et al. (1999)
calculated the distribution of oxygen stores in king penguins
(Table 2) using their
relatively small air volume of 69 ml O2 kg-1, which was
measured from restrained king penguins during simulated dives of up to 136m.
Kooyman and Ponganis (1998)
calculated the distribution in Adélie penguins
(Table 2), assuming that they
had a respiratory volume of 165 ml O2 kg-1
(Kooyman et al., 1973). In the
present study, maximum air volume for each species was larger than in previous
reports. Assuming that our estimated air volumes (125 ml kg-1 for
king; 200 ml kg-1 for Adélie) represent their respiratory
volumes, the total body oxygen and the distribution of oxygen stores are
modified as shown in Table 2.
These are maximum values for the respiratory oxygen stored when the birds
carry the maximum air volume in their respiratory system. As noted by Ponganis
et al. (1999) and Stephenson
(1995), the air volume becomes
greater during unrestrained conditions. To improve the accuracy of this
approach, more research is required into several variables, including (1) the
air volume trapped in the feathers; (2) the tidal volume for each species; (3)
the anatomical volume of the respiratory system of penguins; (4) the amount of
air lost from the respiratory system and plumage during dives.

Regulation of air volume

The positive relationship between dive depth and estimated air volume
during the late phase of ascending in both species
(Fig. 5) implies that penguins
control their air volume. This could be acheived by alterations in inhaled air
volume and in the volume of air trapped in plumage. Stephenson
(1995) found that the
increasing relative influence of the air in the respiratory system on buoyancy
was due to the loss of 47 % of the air in the plumage layer during a dive (1.5
m depth, 11.9s mean duration). In the present study, air volume was estimated
using data obtained during the latter part of the ascent. The air volume
trapped in the plumage is unknown; however, the positive relationship between
air volume and dive depth suggests that penguins might control their inhaled
air volume according to their intended dive depth.

The air associated with the body makes diving birds buoyant, so many
species must use considerable energy to swim against this buoyancy in order to
remain submerged (Stephenson et al.,
1989; Lovvorn and Jones,
1991a,b;
Lovvorn et al., 1991;
Wilson et al., 1992;
Stephenson, 1994). Some flying
birds such as cormorants and ducks have been observed to dive following
expiration (Ross, 1976;
Butler and Woakes, 1979;
Tome and Wrubleski, 1988), so
as to reduce buoyant resistance during dives. However, some penguins have been
observed to dive on inspiration (Kooyman
et al., 1971) and the present study partly supports this
observation at least for deep dives (Fig.
5). The behavioral difference between flying birds and penguins
could be attributed to differences in dive depth and in plumage air volumes
(Wilson et al., 1992).
Penguins generally dive much deeper than flying birds, which means that they
spend much of the dive deeper than the critical depth at which air volume is
so compressed that the buoyant force is negligible. Deep-diving penguins were
not affected by buoyancy in the vicinity of the dive bottom, which explains
why deep diving penguins inhale much air at the beginning of the dive. The
lower estimated air volume during shallower dives
(Fig. 5) further supports this
idea. Here, penguins reduce the volume of air so as to avoid buoyant
resistance during shallow dives.

Loggerhead turtles Caretta caretta adjust their residence depth to
the depth of neutral buoyancy, which varies with the air volume in the
respiratory system in order to minimize cost (Minamikawa et al.,
1997,
2000). In the case of harbor
porpoises Phocoena phocoena, the deeper the dive depth the faster the
initial descent rate, which suggests that porpoises anticipate the depth to
which they will dive before initiating the dive itself
(Otani et al., 1998). The same
pattern was found in penguins (see Wilson,
1995, for a review). Importantly, the present study indicates that
penguins control their inhaled air volume according to the intended dive
depth. This means that diving animals may adapt their diving strategy within
their own biomechanical and physiological constraints.

ACKNOWLEDGEMENTS

We thank Y. Ropert-Coudert, G. Froget and the 1995/96 summer team in
Crozet, and D. Rodary, W. Bonneau and the 1996/97 summer team in Dumont
d'Urville French station, for their assistance in the field, T. Akamatsu,
National Research Institute of Fisheries Engineering, for experiments to test
the performance of the speed data loggers, and R. Wilson and two anonymous
referees for reviewing the manuscript and their helpful suggestions. Aquarium
investigations were done by permission of Tokyo Sea Life Park, Port of Nagoya
Public Aquarium and Kamogawa Sea World. After approval by the ethics committee
of the Institute Français pour la Recherche et la Technologie Polaires
(IFRTP), this study was supported by grants from IFRTP, Centre National de la
Recherche Scientifique (CNRS), Grants-in-Aid for International Scientific
Research from the Ministry of Education, Science, Sports and Culture, and by
the Japan Society for Promotion of the Science for Young Scientists. This
study was conducted through the SIPENS (Sea Ice and Penguin Study)
program.